Evaluation of an alternative in vitro test battery for detecting reproductive toxicants in a grouping context

Reproductive Toxicology

Volumn 55, Issue , 2015, Pages 11-19

  Kroese, E Dinant ^a   Bosgra, Sieto ^a   Buist, Harrie E ^a   Lewin, Geertje ^e   van der Linden, Sander C ^f   Man, Hai yen ^f   Piersma, Aldert H ^b,c   Rorije, Emiel ^c   Schulpen, Sjors H W ^b   Schwarz, Michael ^d   Uibel, Frederik ^d   van Vugt Lussenburg, Barbara M A ^f   Wolterbeek, Andre P M ^a   van der Burg, Bart ^f  

^a TNO   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^d UNIVERSITY OF TÜBINGEN   (Germany)

^e FRAUNHOFER INSTITUTE FOR TOXICOLOGY AND EXPERIMENTAL MEDICINE   (Germany)

^f BIODETECTION SYSTEMS B V   (Netherlands)

Author keywords

Alternative model; CALUX; Developmental toxicity; Embryonic stem cell test; Grouping; Read across; ReProGlo; Zebrafish embryotoxicity assay

Indexed keywords

2 ETHYLHEXANOIC ACID; 2 METHYLHEXANOIC ACID; DIBUTYLTIN DICHLORIDE; MONOBUTYLTIN TRICHLORIDE; MONOETHYLHEXYL PHTHALATE; MONOMETHYL PHTHALATE; TOXIC SUBSTANCE; TRIBUTYLTIN CHLORIDE; UNCLASSIFIED DRUG; VALPROIC ACID; ESTROGEN RECEPTOR; TERATOGENIC AGENT;

ANALYTIC METHOD; ANIMAL CELL; ARTICLE; ASSAY; CALUX BATTERY; CHEMICAL ANALYSIS; CHEMICAL PROCEDURES; CHEMICAL STRUCTURE; CONTROLLED STUDY; DEVELOPMENTAL TOXICITY; DOSIMETRY; EMBRYONIC STEM CELL TEST; EMBRYOTOXICITY; FERTILIZATION; IN VITRO STUDY; MORPHOLOGY; MOUSE; NONHUMAN; REPROGLO ASSAY; TOXICOKINETICS; ZEBRAFISH EMBRYOTOXICITY TEST; ANIMAL; ANIMAL EMBRYO; ANIMAL TESTING ALTERNATIVE; CELL CULTURE; CELL LINE; CLASSIFICATION; DRUG EFFECTS; EMBRYOLOGY; EMBRYONIC STEM CELL; HUMAN; METABOLISM; PROCEDURES; REPORTER GENE; REPRODUCTION; TOXICITY TESTING; ZEBRA FISH;

ANIMALIA; DANIO RERIO;

ANIMAL TESTING ALTERNATIVES; ANIMALS; CELL LINE; CELLS, CULTURED; EMBRYO, NONMAMMALIAN; EMBRYONIC STEM CELLS; GENES, REPORTER; HUMANS; MICE; RECEPTORS, ESTROGEN; REPRODUCTION; TERATOGENS; TOXICITY TESTS; TOXICOKINETICS; ZEBRAFISH;

EID: 84937916430     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2014.10.003     Document Type: Article

References (58)

1. European Commission (EC) Regulation (EC) No 1907/2006 of the European Parliament and of the Council of 18 December 2006 concerning the Registration, Evaluation, Authorization and Restriction of Chemicals (REACH), establishing a European Chemicals Agency, amending Directive No 1488/94 as well as Council Directive 76/769/EEC and Commission Directives 91/155/EEC, 93/105/EC and 2000/21/EC. Off J Eur Union L 2007, 136:3-280.
2. Costanza R., Hartung T. Re-evaluation of animal numbers and costs for in vivo tests to accomplish REACH legislation requirements for chemicals - a report by the transatlantic think tank for toxicology. ALTEX 2009, 26:187-208.
3. Adler S., Basketter D., Creton S., Pelkonen O., Van Benthem J., Zuang V., et al. Alternative (non-animal) methods for cosmetics testing: current status and future prospects - 2010. Arch Toxicol 2011, 85:367-485. [Reproductive toxicity: 447-463].
4. Leist M., Hasigawa N., Rovida C., Daneshiam M., Basketter D., Kiber I., et al. Consensus report on the future of animal-free systemic toxicity testing. ALTEX 2014, 31:341-356. [Reproductive toxicity: 350-351].
5. Schenk B., Weimer M., Bremer S., van der Burg B., Cortvrindt R., Freyberger A., et al. The ReProTect Feasibility Study, a novel comprehensive in vitro approach to detect reproductive toxicants. Reprod Toxicol 2010, 30:200-218.
6. Sipes N.S., Martin M.T., Reif D.M., Kleinstreuer N.C., Judson R.S., Singh A.V., et al. Predictive models of prenatal developmental toxicity from ToxCast high throughput screening data. Toxicol Sci 2011, 124(November (1)):109-127.
7. Piersma A.H., Bosgra S., van Duursen M.B.M., Hermsen S.A.B., Jonker L.R.A., Kroese E.D., et al. Evaluation of an alternative in vitro test battery for detecting reproductive toxicants. Reprod Toxicol 2013, 38:53-64.
8. Hermsen S.A., van den Brandhof E.J., van der Ven L.T., Piersma A.H. Relative embryotoxicity of two classes of chemicals in a modified zebrafish embryotoxicity test and comparison with their in vivo potencies. Toxicol In Vitro 2011, 25(April (3)):745-753.
9. Scholz G., Pohl I., Genschow E., Klemm M., Spielmann H. Embryotoxicity screening using embryonic stem cells in vitro: correlation to in vivo teratogenicity. Cells Tissues Organs 1999, 165(3-4):203-211.
10. Uibel F., Mühleisen A., Köhle C., Weimer M., Stummann T.C., Bremer S., et al. ReProGlo: a new stem cell-based reporter assay aimed to predict embryotoxic potential of drugs and chemicals. Reprod Toxicol 2010, 30(August (1)):103-112.
11. van Duursen M.B., Nijmeijer S.M., Ruchirawat S., van den Berg M. Chemopreventive actions by enterolactone and 13 VIOXX-related lactone derivatives in H295R human adrenocortical carcinoma cells. Toxicol Lett 2010, 192(February (3)):271-277.
12. Hecker M., Hollert H., Cooper R., Vinggaard A.M., Akahori Y., Murphy M., et al. The OECD validation program of the H295R steroidogenesis assay: phase 3 final inter-laboratory validation study. Environ Sci Pollut Res Int 2011, 18(March (3)):503-515.
13. Sonneveld E., Jansen H.J., Riteco J.A.C., Brouwer A., Van der Burg B. Development of androgen- and estrogen-responsive bioassays, members of a panel of human cell line-based highly selective steroid responsive bioassays. Toxicol Sci 2005, 83:136-148.
14. Van der Burg B., Van der Linden S.C., Man H.Y., Winter R., Jonker L., Lussenberg B., et al. A panel of quantitative CALUX® reporter gene assays for reliable high throughput toxicity screening of chemicals and complex mixtures. High throughput screening methods in toxicity testing 2013, 519-532. John Wiley and Sons, Inc., New York. P. Steinberg (Ed.).
15. Daston G.P., Chapin R.E., Scialli A.R., Piersma A.H., Carney E.W., Rogers J.M., et al. A different approach to validating screening assays for developmental toxicity. Birth Defects Res 2010, 89:526-530.
16. Wu S., Fisher J., Nacliff J., Laufersweiler M., Lester C., Daston G., et al. Framework for identifying chemicals with structural features associated with the potential to act as developmental or reproductive toxicants. Chem Res Toxicol 2013, 26:1840-1861.
17. Van der Burg B., Kroese E.D., Piersma A.H. Towards a pragmatic alternative testing strategy for the detection of reproductive toxicants. Reprod Toxicol 2011, 31(May (4)):558-561.
18. van Dartel D.A., Zeijen N.J., de la Fonteyne L.J., van Schooten F.J., Piersma A.H. Disentangling cellular proliferation and differentiation in the embryonic stem cell test, and its impact on the experimental protocol. Reprod Toxicol 2009, 28(September (2)):254-261.
19. Beker van Woudenberg A., Wolterbeek A., Ter Brake L., Snel C., Menke A., Rubingh C., et al. A category approach to predicting the developmental (neuro)toxicity of organotin compounds: the value of the zebrafish (Danio rerio) embryotoxicity test ZET. Reprod Toxicol 2013, 41:35-44.
20. OECD Guideline for the testing of chemicals. Draft proposal for a new guideline Fish Embryo Toxicity (FET) test 2006.
21. Legler J., Van den Brink C.E., Brouwer A., Murk A.J., Van der Saag P.T., Vethaak A.D., et al. Development of a stably transfected estrogen receptor-mediated luciferase reporter gene assay in the human T47-D breast cancer cell line. Toxicol Sci 1999, 48:55-66.
22. Garrison P.M., Tullis K., Aarts J.M.M.J.G., Brouwer A., Giesy J.P., Denison M.S. Fund. Appl Toxicol 1996, 30:194-203.
23. Gauggel S., Derreza-Greven C., Wimmer J., Wingfield M., Van der Burg B., Dietrich D.R. Characterization of biologically available wood combustion particles in cell culture medium. ALTEX 2012, 29(2):183-200.
24. Pieterse B., Felzel E., Winter R., van der Burg B., Brouwer A. PAH-CALUX, an optimized bioassay for carcinogenic hazard identification of polycyclic aromatic hydrocarbons (PAHs) as individual compounds and in complex mixtures. Environ Sci Technol 2013, 47(20):11651-11659.
25. Gijsbers L., van Eekelen H., de Haan L.H., Swier J.M., Heijnk N.L., Kloet S.K., et al. Induction of peroxisome proliferator-activated receptor γ(PPARγ)-mediated gene expression by tomato (Solanum lycopersicum L.) extracts. J Agric Food Chem 2013, 61:3419-3427.
26. Gijsbers L., Man H.Y., Van Eekelen H., De Haan L., Keijer J., Aarts J.M., et al. Induction of peroxisome proliferator-activated receptor γ (PPARγ)-mediated gene expression by extracts of tomato. J Agric Food Chem 2013, 61(14):3419-3427.
27. Van Vugt-Lussenburg B., Besselink H.T., van der Burg B., Brouwer A. Dr-Calux®: a high-throughput screening assay for the detection of dioxin and dioxin-like compounds in food and feed. High-throughput screening methods in toxicity testing 2013, 533-546. John Wiley & Sons Inc., New Jersey, US, [chapter 29]. P. Steinberg (Ed.).
28. Van der Linden S.C., von Bergh A.R.M., Van Vugt-Lussenburg B., Jonker L., Brouwer A., Teunis M., et al. Development of a panel of high throughput reporter gene assays to detect genotoxicity and oxidative stress. Mutat Res Genet Toxicol Environ Mutagen 2013, 760:23-32.
29. OECD Test guideline No.455. Stably transfected human estrogen receptor-transcriptional activation assay for detection of estrogenic agonist-activity of chemicals 2009, Organisation for Economic Cooperation and Development, Paris.
30. Scott W.J., Collins M.D., Nau H. Pharmacokinetic determinants of embryotoxicity in rats associated with organic acids. Environ Health Perspect 1994, 102:97-101.
31. Bosgra S., Westerhout J. Interpreting in vitro developmental toxicity test battery results: the consideration of toxicokinetics. Reprod Toxicol 2015, 55:73-80.
32. Hermann K. Effects of the anticonvulsant drug valproic acid and related substances on the early development of the zebrafish (Brachydanio Rerio). Toxicol In Vitro 1993, 7:41-54.
33. Robert E. Valproic acid and spina bifida. Lancet 1982, 2:1096.
34. Kavlock R., Boekelheide K., Chapin R., Cunningham M., Faustman E., Foster P., et al. NTP Center for the Evaluation of Risks to Human Reproduction: phthalates expert panel report on the reproduction and developmental toxicity of di(2-ethylhexyl) phthalate. Reprod Toxicol 2002, 16:529-653.
35. Krug A.K., Kolde R., Gaspar J.A., Rempel E., Balmer N.V., Meganathan K., et al. Human embryonic stem cell-derived test systems for developmental neurotoxicity: a transcriptomics approach. Arch Toxicol 2013, 87(1):123-143.
36. Zimmer B., Pallocca G., Dreser N., Foerster S., Waldmann T., Westerhout J., et al. Profiling of drugs and environmental chemicals for functional impairment of neural crest migration in a novel stem cell-based test battery. Arch Toxicol 2014, 88(5):1109-1126.
37. Mandula H., Parepally J.M., Feng R., Smith Q.R. Role of site-specific binding to plasma albumin in drug availability to brain. J Pharmacol Exp Ther 2006, 317(2):667-675.
38. Semmes R.L., Shen D.D. Nonlinear binding of valproic acid (VPA) and E-delta 2-valproic acid to rat plasma proteins?. Pharm Res 1990, 7(5):461-467.
39. OECD Environment Health and Safety Publications, Series on Testing and Assessment No. 80, Guidance on grouping of chemicals 2007.
40. Binkerd P.E., Rowland J.M., Nau H., Hendrickx A.G. Evaluation of valproic acid (VPA) developmental toxicity and pharmacokinetics in Sprague-Dawley rats. Fundam Appl Toxicol 1988, 11:485-493.
41. Narotsky M.G., Kavlock E.Z. Developmental toxicity and structure-activity relationships of aliphatic acids, including dose-response assessment of valproic acid in mice and rats. Fundam Appl Toxicol 1994, 22:251-265.
42. Fabian E., Hulzebos E., Mennes W., Piersma A.H. A category approach for reprotoxic effects of phthalates. Crit Rev Toxicol 2006, 36:695-726.
43. Lyche J.L., Gutleb A.C., Bergman A., Eriksen G.S., Murk A.J., Ropstad E., et al. Reproductive and developmental toxicity of phthalates. J Toxicol Environ Health B Crit Rev 2009, 12:225-249.
44. Kwack S.J., Kim K.B., Kim H.S., Lee B.M. Comparative toxicological evaluation of phthalate diesters and metabolites in Sprague-Dawley male rats for risk assessment. J Toxicol Environ Health 2009, 72:1446-1454.
45. Ema M., Miyawaki E. Effects on development of the reproductive system in male offspring of rats given butyl benzyl phthalate during late pregnancy. Reprod Toxicol 2002, 16:71-76.
46. Saillenfait A.M., Sabate J.P., Gallissot F. Comparative embryo-toxicities of butyl benzyl phthalate, mono-n-butyl phthalate and mono-benzyl phthalate in mice and rats: in vivo and in vitro observations. Reprod Toxicol 2003, 17:575-583.
47. Gray L.E., Ostby J., Furr J., Pricwe M., Veeramachaneni D.N.R., Parks L. Exposure to the phthalates DEHP, BBP, and DINP, but not DEP, DMP, or DOTP, alters sexual differentiation of the male rat. Toxicol Sci 2000, 58:350-365.
48. Schwetz B.A., Harris M.W. Developmental toxicology: status of the field and contribution of the National Toxicology Program. Environ Health Perspect 1993, 100:269-282.
49. Genschow E., Spielmann H., Scholz G., Seiler A., Brown N., Piersma A., et al. The ECVAM international validation study on in vitro embryotoxicity tests: results of the definitive phase and evaluation of prediction models. ATLA 2002, 30:151-176.
50. Heidrich D.D., Steckelbroeck S., Klingmuller D. Inhibition of human cytochrome P450 aromatase activity by butyltins. Steroids 2001, 66(10):763-769.
51. Cooke G.M. Effect of organotins on human aromatase activity in vitro. Toxicol Lett 2002, 126(2):121-130.
52. Lo S., Alléra A., Albers P., Heimbrecht J., Jantzen E., Klingmüller D., et al. Dithioerythritol (DTE) prevents inhibitory effects of triphenyltin (TPT) on the key enzymes of the human sex steroid hormone metabolism. J Steroid Biochem Mol Biol 2003, 84(5):569-576.
53. World Health Organization (WHO) Mono-and disubstituted methyltin, butyltin, and octyltin compounds. Concise international chemical assessment document 2006, 73.
54. Ema M., Arima A., Fukunishi K., Matsumoto M., Hirata-Koizumi M., Hirose A., et al. Developmental toxicity of dibutyltin dichloride given on three consecutive days during organogenesis in cynomolgus monkeys. Drug Chem Toxicol 2009, 32:150-157.
55. Noda T., Morita S., Yamano T., Shimizu M., Nakamura T., Saitoh M., et al. Teratogenicity study of tri-n-butyltin acetate in rats by oral administration. Toxicol Lett 1991, 55:109-115.
56. Ema M., Harazono A., Miyawaki E., Ogawa Y. Effect of the day of administration on the developmental toxicity of tributyltin chloride in rats. Arch Environ Contam Toxicol 1997, 33:90-96.
57. Rotroff D.M., Wetmore B.A., Dix D.J., Ferguson S.S., Clewell H.J., Houck K.A., et al. Incorporating human dosimetry and exposure into high-throughput in vitro toxicity screening. Toxicol Sci 2010, 117(2):348-358.
58. Wambaugh J., Strope C., Nicolas C., Pearce R., Judson R., Goldsmith R. High throughput pharmacokinetics for environmental chemicals. Poster presentation, society of toxicology's 53rd annual meeting 2014, [in preparation].